Vitamin D supplementation and Covid‐19 outcomes: A systematic review, meta‐analysis and meta‐regression
Timotius Ivan Hariyanto, Denny Intan, Joshua Edward Hananto, Harapan Harapan, Andree Kurniawan
Reviews in Medical Virology, doi:10.1002/rmv.2269
Vitamin D has many protective properties and potential role against acute lung injury. Low serum vitamin D is associated with high risk of pneumonia and development of acute respiratory distress syndrome. This study sought to analyse the efficacy of vitamin D in improving the outcomes of coronavirus disease 2019 (Covid-19) patients. Using specific keywords, we comprehensively searched the potential articles on PubMed, Europe PMC and ClinicalTrials.gov database until 8th May 2021. All published studies on Covid-19 and vitamin D were retrieved. Statistical analysis was conducted using Review Manager 5.4 software. A total of 11 studies with 22,265 Covid-19 patients were included in the meta-analysis. Our data suggested that vitamin D supplementation was associated with reduction in intensive care unit admission rate (OR 0.27; 95% CI: 0.09-0.76, p = 0.010, I 2 = 70%, random-effect modelling); reduction of the need for mechanical ventilation (OR 0.34; 95% CI: 0.16-0.72, p = 0.005, I 2 = 61%, random-effect modelling) and reduction of mortality from Covid-19 (OR 0.37; 95% CI: 0.21-0.66, p < 0.001, I 2 = 50%, random-effect modelling). Further analysis showed that the associations were influenced by age (p = 0.020). Our study suggests that vitamin D supplementation may offer beneficial effects on Covid-19 outcomes. However, more randomized clinical trials are required to confirm this conclusion. K E Y W O R D S coronavirus disease 2019, Covid-19, vitamin D 1 | INTRODUCTION Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection continues to spread globally causing a pandemic and has become a major medical focus for the last couple of years. The pandemic has involved over 164 million confirmed cases, with more than 3.4 million deaths as of 23 May 2021. 1 While some SARS-CoV-2 infections appear as mild upper respiratory symptoms and may be self-limiting, notable numbers of patients require hospitalizations and intensive treatment following progression into a more severe cases,
CONFLICT OF INTEREST The authors declare that there is no conflict of interest.
AUTHOR CONTRIBUTION
Conceptualization
References
Annweiler, Corvaisier, Gautier, Vitamin D supplementation associated to better survival in hospitalized frail elderly COVID-19 patients: the GERIA-COVID quasi-experimental study, Nutrients,
doi:10.3390/nu12113377
Annweiler, Hanotte, De L'eprevier, Sabatier, Lafaie et al., Vitamin D and survival in COVID-19 patients: a quasiexperimental study, J Steroid Biochem Mol Biol,
doi:10.1016/j.jsbmb.2020.105771
Begg, Mazumdar, Operating characteristics of a rank correlation test for publication bias, Biometrics
Buonaguro, Ascierto, Morse, Covid-19: time for a paradigm change, Rev Med Virol,
doi:10.1002/rmv.2134
Cangiano, Fatti, Danesi, Mortality in an Italian nursing home during COVID-19 pandemic: correlation with gender, age, ADL, vitamin D supplementation, and limitations of the diagnostic tests, Aging (Albany NY),
doi:10.18632/aging.202307
Castillo, Costa, Barrios, Effect of calcifediol treatment and best available therapy versus best available therapy on intensive care unit admission and mortality among patients hospitalized for COVID-19: a pilot randomized clinical study, J Steroid Biochem Mol Biol,
doi:10.1016/j.jsbmb.2020.105751
Daneshkhah, Agrawal, Eshein, Subramanian, Roy et al., Evidence for possible association of vitamin D status with cytokine storm and unregulated inflammation in COVID-19 patients, Aging Clin Exp Res,
doi:10.1007/s40520-020-01677%2Dy
Giannini, Passeri, Tripepi, Effectiveness of in-hospital cholecalciferol use on clinical outcomes in comorbid COVID-19 patients: a hypothesis-generating study, Nutrients,
doi:10.3390/nu13010219
Gong, Dong, Xia, Correlation analysis between disease severity and inflammation-related parameters in patients with COVID-19: a retrospective study, BMC Infect Dis,
doi:10.1186/s12879-020-05681-5
Grant, Lahore, Mcdonnell, Evidence that vitamin D supplementation could reduce risk of influenza
Hariyanto, Christian, Kurniawan, Human immunodeficiency virus and mortality from coronavirus disease 2019: a systematic review and meta-analysis, South Afr J HIV Med,
doi:10.4102/sajhivmed.v22i1.1220
Hariyanto, Halim, Gunawan, Kurniawan, Ivermectin and outcomes from Covid-19 pneumonia: a systematic review and meta-analysis of randomized clinical trial studies, Rev Med Virol,
doi:10.1002/rmv.2265
Hariyanto, Halim, Jodhinata, Yanto, Kurniawan, Colchicine treatment can improve outcomes of coronavirus disease 2019 (COVID-19): a systematic review and meta-analysis, Clin Exp Pharmacol Physiol,
doi:10.1111/1440-1681.13488
Hariyanto, Hardyson, Kurniawan, Efficacy and safety of tocilizumab for coronavirus disease 2019 (Covid-19) patients: a systematic review and meta-analysis, Drug Res (Stuttg),
doi:10.1055/a%2D1336-2371
Hariyanto, Japar, Damay, Kwenandar, Sieto, Kurniawan A. The use of ACE inhibitor/ARB in SARS-CoV-2 patients: a comprehensive narrative review, Asian J Med Sci,
doi:10.3126/ajms.v11i6.29911
Hariyanto, Japar, Kwenandar, Inflammatory and hematologic markers as predictors of severe outcomes in COVID-19 infection: a systematic review and meta-analysis, Am J Emerg Med,
doi:10.1016/j.ajem.2020.12.076
Hariyanto, Kurniawan, Dipeptidyl peptidase 4 (DPP4) inhibitor and outcome from coronavirus disease 2019 (COVID-19) in diabetic patients: a systematic review, meta-analysis, and meta-regression, J Diabetes Metab Disord,
doi:10.1007/s40200-021-00777-4
Hariyanto, Kurniawan, Obstructive sleep apnea (OSA) and outcomes from coronavirus disease 2019 (COVID-19) pneumonia: a systematic review and meta-analysis, Sleep Med,
doi:10.1016/j.sleep.2021.03.029
Hariyanto, Kurniawan, Tocilizumab administration is associated with the reduction in biomarkers of coronavirus disease 2019 infection, J Med Virol,
doi:10.1002/jmv.26698
Hariyanto, None
Hariyanto, Putri, Situmeang, Kurniawan, Dementia is associated with severe coronavirus disease 2019 (COVID-19) infection, Am J Med Sci,
doi:10.1016/j.amjms.2020.10.026
Hariyanto, Rizki, Kurniawan, Anosmia/Hyposmia is a good predictor of coronavirus disease 2019 (COVID-19) infection: a meta-analysis, Int Arch Otorhinolaryngol,
doi:10.1055/s%2D0040-1719120
Hashemi, Thijssen, Hosseini, Tabarraei, Pourkarim et al., Human gene polymorphisms and their possible impact on the clinical outcome of SARS-CoV-2 infection, Arch Virol,
doi:10.1007/s00705-021-05070-6
Hernández, Nan, Fernandez-Ayala, Vitamin D status in hospitalized patients with SARS-CoV-2 infection, J Clin Endocrinol Metab,
doi:10.1210/clinem/dgaa733
Huang, Wang, Chen, Song, Liu et al., Perioperative antibiotics to prevent acute endophthalmitis after ophthalmic surgery: a systematic review and meta-analysis, PLoS One,
doi:10.1371/journal.pone.0166141
Jain, Chaurasia, Sengar, Singh, Mahor et al., Analysis of vitamin D level among asymptomatic and critically ill COVID-19 patients and its correlation with inflammatory markers, Sci Rep,
doi:10.1038/s41598-020-77093%2Dz
Jayawardena, Jeyakumar, Francis, Misra, Impact of the vitamin D deficiency on COVID-19 infection and mortality in Asian countries, Diabetes Metab Syndr,
doi:10.1016/j.dsx.2021.03.006
Jevalikar, Mithal, Singh, Lack of association of baseline 25-hydroxyvitamin D levels with disease severity and mortality in Indian patients hospitalized for COVID-19, Sci Rep,
doi:10.1038/s41598-021-85809%2Dy
Kralj, Jakovac, Vitamin D and COVID-19 in an immunocompromised patient with multiple comorbidities-A Case Report, Clin Case Rep,
doi:10.1002/ccr3.4010
Laplana, Royo, Fibla, Hariyanto, Intan et al., Vitamin D supplementation and Covid-19 outcomes: a systematic review, meta-analysis and meta-regression, Rev Med Virol
Ling, Broad, Murphy, High-dose cholecalciferol booster therapy is associated with a reduced risk of mortality in patients with COVID-19: a cross-sectional multi-centre observational study, Nutrients,
doi:10.3390/nu12123799
Mahdavi, A brief review of interplay between vitamin D and angiotensin-converting enzyme 2: implications for a potential treatment for COVID-19, Rev Med Virol,
doi:10.1002/rmv.2119
Mcnally, Sampson, Matheson, Hutton, Little, Vitamin D receptor (VDR) polymorphisms and severe RSV bronchiolitis: a systematic review and meta-analysis, Pediatr Pulmonol,
doi:10.1002/ppul.22877
Mokhtari, Hassani, Ghaffari, Ebrahimi, Yarahmadi, Hassanzadeh G. COVID-19 and multiorgan failure: a narrative review on potential mechanisms, J Mol Histol,
doi:10.1007/s10735-020-09915-3
Murai, Fernandes, Sales, Effect of a single high dose of vitamin D3 on hospital length of stay in patients with moderate to severe COVID-19: a randomized clinical trial, J Am Med Assoc,
doi:10.1001/jama.2020.26848
Murdaca, Pioggia, Negrini, Vitamin D and Covid-19: an update on evidence and potential therapeutic implications, Clin Mol Allergy,
doi:10.1186/s12948-020-00139-0
Pereira, Damascena, Azevedo, De Almeida Oliveira, Da et al., Vitamin D deficiency aggravates COVID-19: systematic review and meta-analysis, Crit Rev Food Sci Nutr,
doi:10.1080/10408398.2020.1841090
Putri, Hariyanto, Hananto, Christian, Situmeang et al., Parkinson's disease may worsen outcomes from coronavirus disease 2019 (COVID-19) pneumonia in hospitalized patients: a systematic review, meta-analysis, and meta-regression
Qin, Zhou, Hu, Dysregulation of immune response in patients with coronavirus, Clin Infect Dis,
doi:10.1093/cid/ciaa248
Schwalfenberg, A review of the critical role of vitamin D in the functioning of the immune system and the clinical implications of vitamin D deficiency, Mol Nutr Food Res,
doi:10.1002/mnfr.201000174
Tan, Ho, Kalimuddin, Cohort study to evaluate the effect of vitamin D, magnesium, and vitamin B12 in combination on progression to severe outcomes in older patients with coronavirus (COVID-19), Nutrition,
doi:10.1016/j.nut.2020.111017
Terrin, Schmid, Lau, Olkin, Adjusting for publication bias in the presence of heterogeneity, Stat Med,
doi:10.1002/sim.1461
Van Harten, Van Woudenbergh, Van Dijk, Haagsman, Cathelicidins: immunomodulatory antimicrobials. Vaccines (Basel),
doi:10.3390/vaccines6030063
Vasheghani, Jannati, Baghaei, Rezaei, Marjani, The association of 25 (OH) vitamin D levels and severity and outcome of COVID-19: a cross-sectional study,
doi:10.21203/rs.3.rs%2D141034/v1
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